THE TOXIC DINOFLAGELLATE GYMNODINIUM CATENATUM (DINOPHYCEAE) REQUIRES MARINE BACTERIA FOR GROWTH1

Interactions with the bacterial community are increasingly considered to have a significant influence on marine phytoplankton populations. Here we used a simplified dinoflagellate‐bacterium experimental culture model to conclusively demonstrate that the toxic dinoflagellate Gymnodinium catenatum H. W. Graham requires growth‐stimulatory marine bacteria for postgermination survival and growth, from the point of resting cyst germination through to vegetative growth at bloom concentrations (10³ cells · mL^?1). Cysts of G. catenatum were germinated and grown in unibacterial coculture with antibiotic‐resistant or antibiotic‐sensitive Marinobacter sp. DG879 or Brachybacterium sp., and with mixtures of these two bacteria. Addition of antibiotics to cultures grown with antibiotic‐sensitive strains of bacteria resulted in death of the dinoflagellate culture, whereas cultures grown with antibiotic‐resistant bacteria survived antibiotic addition and continued to grow beyond the 21 d experiment. Removal of either bacterial type from mixed‐bacterial dinoflagellate cultures (using an antibiotic) resulted in cessation of dinoflagellate growth until bacterial concentration recovered to preaddition concentrations, suggesting that the bacterial growth factors are used for dinoflagellate growth or are labile. Examination of published reports of axenic dinoflagellate culture indicate that a requirement for bacteria is not universal among dinoflagellates, but rather that species may vary in their relative reliance on, and relationship with, the bacterial community. The experimental model approach described here solves a number of inherent and logical problems plaguing studies of algal‐bacterium interactions and provides a flexible and tractable tool that can be extended to examine bacterial interactions with other phytoplankton species.     

Algicidal bacteria in the sea and their impact on algal blooms

Over the past two decades, many reports have revealed the existence of bacteria capable of killing phytoplankton. These algicidal bacteria sometimes increase in abundance concurrently with the decline of algal blooms, suggesting that they may affect algal bloom dynamics. Here, we synthesize the existing knowledge on algicidal bacteria interactions with marine eukaryotic microalgae. We discuss the effectiveness of the current methods to characterize the algicidal phenotype in an ecosystem context. We briefly consider the literature on the phylogenetic identification of algicidal bacteria, their interaction with their algal prey, the characterization of algicidal molecules, and the enumeration of algicidal bacteria during algal blooms. We conclude that, due to limitations of current methods, the evidence for algicidal bacteria causing algal bloom decline is circumstantial. New methods and an ecosystem approach are needed to test hypotheses on the impact of algicidal bacteria in algal bloom dynamics. This will require enlarging the scope of inquiry from its current focus on the potential utility of algicidal bacteria in the control of harmful algal blooms. We suggest conceptualizing bacterial algicidy within the general problem of bacterial regulation of algal community structure in the ocean.     

Comparative composition and dynamics of harmful dinoflagellates in Mediterranean salt marshes and nearby external marine waters

The taxonomic structure of phytoplankton populations in two Mediterranean coastal lagoons were compared with those of nearby marine waters (external waters). Mediterranean confined lagoons remain isolated for most the year and concentrate phytoplankton to a very high biomass. Coastal lagoons on the Mediterranean may, therefore, act as accumulators of neritic phytoplankton (including species related to harmful algal blooms). We examined whether coastal lagoons act as concentrators of marine toxic dinoflagellates during confinement periods, and the common environmental factors that favour growth of specific harmful species in the two ecosystems considered: coastal lagoons and external waters. An alternation between the dominance of diatoms and dinoflagellates was observed, coinciding with that described in Margalef's mandala, occurring in external waters as well as in coastal lagoons. Moreover, the temporal patter was different in the two ecosystems. Dinoflagellate species composition and their bloom period were highly variable in time and space, thus, species had to be analysed individually. Most of the dinoflagellate species found in this study were potentially harmful and high biomass producers. Harmful dinoflagellate species performed well in both, external waters and lagoons, but the specific species-dependent affinity to each of these environments determined which organisms bloom there. Thus, expansion of harmful algal blooms (HAB) to inland waters is not likely and some environmental factors such as the oxidised state of available nitrogen, became determinant to the success and bloom of a species in the coastal lagoon ecosystem.     

BACTERIA‐INDUCED MOTILITY REDUCTION IN LINGULODINIUM POLYEDRUM (DINOPHYCEAE)1

Biotic factors that affect phytoplankton physiology and behavior are not well characterized but probably play a crucial role in regulating their population dynamics in nature. We document evidence that some marine bacteria can decrease the swimming speed of motile phytoplankton through the release of putative protease(s). Using the dinoflagellate Lingulodinium polyedrum (F. Stein) J. D. Dodge as a model system, we showed that the motility‐reducing components of bacterial‐algal cocultures were mostly heat labile, were of high molecular weight (>50 kDa), and could be partially neutralized by incubations with protease inhibitors. We further showed that additions of the purified protease pronase E decreased dinoflagellate swimming speed in a concentration‐dependent manner. We propose that motility can be used as a marker for dinoflagellate stress or general unhealthy status due to proteolytic bacteria, among other factors.     

Bacterial community associated with Pfiesteria-like dinoflagellate cultures

Dinoflagellates (Eukaryota; Alveolata; Dinophyceae) are single-cell eukaryotic microorganisms implicated in many toxic outbreaks in the marine and estuarine environment. Co-existing with dinoflagellate communities are bacterial assemblages that undergo changes in species composition, compete for nutrients and produce bioactive compounds, including toxins. As part of an investigation to understand the role of the bacteria in dinoflagellate physiology and toxigenesis, we have characterized the bacterial community associated with laboratory cultures of four ' Pfiesteria -like' dinoflagellates isolated from 1997 fish killing events in Chesapeake Bay. A polymerase chain reaction with oligonucleotide primers specific to prokaryotic 16S rDNA gene sequences was used to characterize the total bacterial population, including culturable and non-culturable species, as well as possible endosymbiotic bacteria. The results indicate a diverse group of over 30 bacteria species co-existing in the dinoflagellate cultures. The broad phylogenetic types of dinoflagellate-associated bacteria were generally similar, although not identical, to those bacterial types found in association with other harmful algal species. Dinoflagellates were made axenic, and the culturable bacteria were added back to determine the contribution of the bacteria to dinoflagellate growth. Confocal scanning laser fluorescence microscopy with 16S rDNA probes was used to demonstrate a physical association of a subset of the bacteria and the dinoflagellate cells. These data point to a key component in the bacterial community being species in the marine alpha-proteobacteria group, most closely associated with the α-3 or SAR83 cluster.     

The impact of associated bacteria on morphology and physiology of the dinoflagellate Alexandrium tamarense

Despite their potential impact on phytoplankton dynamics and biogeochemical cycles, biological associations between algae and bacteria are still poorly understood. The aim of the present work was to characterize the influence of bacteria on the growth and function of the dinoflagellate Alexandrium tamarense. Axenic microalgal cultures were inoculated with a microbial community and the resulting cultures were monitored over a 15-month period, in order to allow for the establishment of specific algal–bacterial associations. Algal cells maintained in these new mixed cultures first experienced a period of growth inhibition. After several months, algal growth and cell volume increased, and indicators of photosynthetic function also improved. Our results suggest that community assembly processes facilitated the development of mutualistic relationships between A. tamarense cells and bacteria. These interactions had beneficial effects on the alga that may be only partly explained by mixotrophy of A. tamarense cells. The potential role of organic exudates in the establishment of these algal–bacterial associations is discussed. The present results do not support a role for algal–bacterial interactions in dinoflagellate toxin synthesis. However, variations observed in the toxin profile of A. tamarense cells during culture experiments give new clues for the understanding of biosynthetic pathways of saxitoxin, a potent phycotoxin.     

Dimethylsulfoniopropionate turnover is linked to the composition and dynamics of the bacterioplankton assemblage during a microcosm phytoplankton bloom

Processing of the phytoplankton-derived organic sulfur compound dimethylsulfoniopropionate (DMSP) by bacteria was studied in seawater microcosms in the coastal Gulf of Mexico (Alabama). Modest phytoplankton blooms (peak chlorophyll a [Chl a] concentrations of approximately 2.5 microg liter(-1)) were induced in nutrient-enriched microcosms, while phytoplankton biomass remained low in unamended controls (Chl a concentrations of approximately 0.34 microg liter(-1)). Particulate DMSP concentrations reached 96 nM in the enriched microcosms but remained approximately 14 nM in the controls. Bacterial biomass production increased in parallel with the increase in particulate DMSP, and nutrient limitation bioassays in the initial water showed that enrichment with DMSP or glucose caused a similar stimulation of bacterial growth. Concomitantly, increased bacterial consumption rate constants of dissolved DMSP (up to 20 day(-1)) and dimethylsulfide (DMS) (up to 6.5 day(-1)) were observed. Nevertheless, higher DMSP S assimilation efficiencies and higher contribution of DMSP to bacterial S demand were found in the controls compared to the enriched microcosms. This indicated that marine bacterioplankton may rely more on DMSP as a source of S under oligotrophic conditions than under the senescence phase of phytoplankton blooms. Phylogenetic analysis of the bacterial assemblages in all microcosms showed that the DMSP-rich algal bloom favored the occurrence of various Roseobacter members, flavobacteria (Bacteroidetes phylum), and oligotrophic marine Gammaproteobacteria. Our observations suggest that the composition of the bacterial assemblage and the relative contribution of DMSP to the overall dissolved organic sulfur/organic matter pool control how efficiently bacteria assimilate DMSP S and thereby potentially divert it from DMS production.     

Identification and characterization of potentially algal-lytic marine bacteria strongly associated with the toxic dinoflagellate Alexandrium catenella

The toxic dinoflagellate Alexandrium catenella isolated from fjords in Southern Chile produces several analogues of saxitoxin and has been associated with outbreaks of paralytic shellfish poisoning. Three bacterial strains, which remained in close association with this dinoflagellate in culture, were isolated by inoculating the dinoflagellate onto marine agar. The phenotypically different cultivable bacterial colonies were purified. Their genetic identification was done by polymerase chain reaction amplification of the 16S rRNA genes. Partial sequence analysis suggested that the most probable affiliations were to two bacterial phyla: Proteobacteria and the Cytophaga group. The molecular identification was complemented by morphological data and biochemical profiling. The three bacterial species, when grown separately from phytoplankton cells in high-nutrient media, released algal-lytic compounds together with aminopeptidase, lipase, glucosaminidase, and alkaline phosphatase. When the same bacteria, free of organic nutrients, were added back to the algal culture they displayed no detrimental effects on the dinoflagellate cells and recovered their symbiotic characteristics. This observation is consistent with phylogenetic analysis that reveals that these bacteria correspond to species distinct from other bacterial strains previously classified as algicidal bacteria. Thus, bacterial-derived lytic activities are expressed only in the presence of high-nutrient culture media and it is likely that in situ environmental conditions may modulate their expression.     

Major differences of bacterial diversity and activity inside and outside of a natural iron-fertilized phytoplankton bloom in the Southern Ocean

One of the first comparisons of a natural iron fertilized bloom with a high-nutrient low-chlorophyll (HNLC) site was undertaken during the Kerguelen ocean and plateau compared study (KEOPS) cruise. To understand better the bacteria–phytoplankton relationship in the context of natural iron fertilization, bacterial diversity and activity was investigated in the bloom and in the adjacent HNLC region by 16S rDNA clone libraries and by single strand conformation polymorphism (SSCP) analysis. Both libraries were dominated by Alphaproteobacteria , Gammaproteobacteria and the Cytophaga-Flavobacteria-Bacteroides group. Cluster analysis at 99% sequence similarity yielded several microdiverse clusters and revealed striking differences between the two libraries. In the bloom, the dominant operational taxonomic units (OTUs) were the Roseobacter NAC11-7 cluster, SAR92 and a Cytophaga-Flavobacteria-Bacteroides cluster related to the agg58 group, whereas in the HNLC region, SAR11, Roseobacter RCA and Polaribacter dominated. SSCP analysis of 16S rDNA and 16S rRNA revealed contrasting dynamics of three different Roseobacter OTUs. Roseobacter NAC11-7 and NAC11-6 had higher relative abundances and activities in the bloom compared with the HNLC site and NAC11-6 was only detected at the decline of the bloom concomitant with a shift in phytoplankton composi tion. In contrast, Roseobacter RCA was relatively abundant and active both inside and outside of the bloom. These results suggest that the different OTUs within the Roseobacter group represent functional groups that each play an important role in the cycling of carbon.     

Planktonic food chains of a highly humic lake

The development and metabolism of the plankton of a highly humic lake were followed over the vernal primary production maximum. The study was made in a mesocosm in which large filter feeders, typical of this lake in summer, were absent. During the rising phase of phytoplankton, the community was predominantly autotrophic. The most important constituents in the algal biomass were a dinoflagellate, Gymnodinium sp. (40–50%), and a prasinophycean, Scourfieldia cordiformis (7%). The biomasses of Chlamydomonas spp. and Chrysococcus spp. reached their maxima a few days later and Cryptomonas sp. became most abundant at the end of the experiment. After the phytoplankton maximum, about one week from the beginning ofthe experiment, grazing of algae by phagotrophic protozoans and phosphate depletion led to a rapid decrease of algal biomass and the community became predominantly heterotrophic. In spite of a large variation in algal biomass and primary production, the biomass of bacteria remained of the same order of magnitude as in algae both before and after the algal maximum. Bacteria were mostly responsible for the plankton respiration, which also showed no dependence on primary production. Since exudation by phytoplankton was also low, the nutrition of bacterioplankton was probably mainly based on allochthonous dissolved organic matter rather than or primary production. Thus the production of bacteria was an additional food source for higher trophic levels along with phytoplankton. Because filter feeding zooplankton was absent in the experiment, protozoans were the only grazers utilizing algae and bacteria. Essentially all growth of bacteria was used by bacterivores.     

Bacterial community structure associated with a dimethylsulfoniopropionate-producing North Atlantic algal bloom

The bacteria associated with oceanic algal blooms are acknowledged to play important roles in carbon, nitrogen, and sulfur cycling, yet little information is available on their identities or phylogenetic affiliations. Three culture-independent methods were used to characterize bacteria from a dimethylsulfoniopropionate (DMSP)-producing algal bloom in the North Atlantic. Group-specific 16S rRNA-targeted oligonucleotides, 16S ribosomal DNA (rDNA) clone libraries, and terminal restriction fragment length polymorphism analysis all indicated that the marine Roseobacter lineage was numerically important in the heterotrophic bacterial community, averaging >20% of the 16S rDNA sampled. Two other groups of heterotrophic bacteria, the SAR86 and SAR11 clades, were also shown by the three 16S rRNA-based methods to be abundant in the bloom community. In surface waters, the Roseobacter, SAR86, and SAR11 lineages together accounted for over 50% of the bacterial rDNA and showed little spatial variability in abundance despite variations in the dominant algal species. Depth profiles indicated that Roseobacter phylotype abundance decreased with depth and was positively correlated with chlorophyll a, DMSP, and total organic sulfur (dimethyl sulfide plus DMSP plus dimethyl sulfoxide) concentrations. Based on these data and previous physiological studies of cultured Roseobacter strains, we hypothesize that this lineage plays a role in cycling organic sulfur compounds produced within the bloom. Three other abundant bacterial phylotypes (representing a cyanobacterium and two members of the alpha Proteobacteria) were primarily associated with chlorophyll-rich surface waters of the bloom (0 to 50 m), while two others (representing Cytophagales and delta Proteobacteria) were primarily found in deeper waters (200 to 500 m).     

sxtA-based quantitative molecular assay to identify saxitoxin-producing harmful algal blooms in marine waters

The recent identification of genes involved in the production of the potent neurotoxin and keystone metabolite saxitoxin (STX) in marine eukaryotic phytoplankton has allowed us for the first time to develop molecular genetic methods to investigate the chemical ecology of harmful algal blooms in situ. We present a novel method for detecting and quantifying the potential for STX production in marine environmental samples. Our assay detects a domain of the gene sxtA that encodes a unique enzyme putatively involved in the sxt pathway in marine dinoflagellates, sxtA4. A product of the correct size was recovered from nine strains of four species of STX-producing Alexandrium and Gymnodinium catenatum and was not detected in the non-STX-producing Alexandrium species, other dinoflagellate cultures, or an environmental sample that did not contain known STX-producing species. However, sxtA4 was also detected in the non-STX-producing strain of Alexandrium tamarense, Tasmanian ribotype. We investigated the copy number of sxtA4 in three strains of Alexandrium catenella and found it to be relatively constant among strains. Using our novel method, we detected and quantified sxtA4 in three environmental blooms of Alexandrium catenella that led to STX uptake in oysters. We conclude that this method shows promise as an accurate, fast, and cost-effective means of quantifying the potential for STX production in marine samples and will be useful for biological oceanographic research and harmful algal bloom monitoring.     

Phylogenetic diversity and specificity of bacteria closely associated with Alexandrium spp. and other phytoplankton

While several studies have suggested that bacterium-phytoplankton interactions have the potential to dramatically influence harmful algal bloom dynamics, little is known about how bacteria and phytoplankton communities interact at the species composition level. The objective of the current study was to determine whether there are specific associations between diverse phytoplankton and the bacteria that co-occur with them. We determined the phylogenetic diversity of bacterial assemblages associated with 10 Alexandrium strains and representatives of the major taxonomic groups of phytoplankton in the Gulf of Maine. For this analysis we chose xenic phytoplankton cultures that (i) represented a broad taxonomic range, (ii) represented a broad geographic range for Alexandrium spp. isolates, (iii) grew under similar cultivation conditions, (iv) had a minimal length of time since the original isolation, and (v) had been isolated from a vegetative phytoplankton cell. 16S rRNA gene fragments of most Bacteria were amplified from DNA extracted from cultures and were analyzed by denaturing gradient gel electrophoresis and sequencing. A greater number of bacterial species were shared by different Alexandrium cultures, regardless of the geographic origin, than by Alexandrium species and nontoxic phytoplankton from the Gulf of Maine. In particular, members of the Roseobacter clade showed a higher degree of association with Alexandrium than with other bacterial groups, and many sequences matched sequences reported to be associated with other toxic dinoflagellates. These results provide evidence for specificity in bacterium-phytoplankton associations.     

Aerobic anoxygenic photosynthesis in Roseobacter clade bacteria from diverse marine habitats

The marine Roseobacter clade comprises several genera of marine bacteria related to the uncultured SAR83 cluster, the second most abundant marine picoplankton lineage. Cultivated representatives of this clade are physiologically heterogeneous, and only some have the capability for aerobic anoxygenic photosynthesis, a process of potentially great ecological importance in the world's oceans. In an attempt to correlate phylogeny with ecology, we investigated the diversity of Roseobacter clade strains from various marine habitats (water samples, biofilms, laminariae, diatoms, and dinoflagellate cultures) by using the 16S rRNA gene as a phylogenetic marker gene. The potential for aerobic anoxygenic photosynthesis was determined on the genetic level by PCR amplification and sequencing of the pufLM genes of the bacterial photosynthesis reaction center and on the physiological level by detection of bacteriochlorophyll (Bchl) a. A collection of ca. 1,000 marine isolates was screened for members of the marine Roseobacter clade by 16S rRNA gene-directed multiplex PCR and sequencing. The 42 Roseobacter clade isolates found tended to form habitat-specific subclusters. The pufLM genes were detected in two groups of strains from dinoflagellate cultures but in none of the other Roseobacter clade isolates. Strains within the first group (the DFL-12 cluster) also synthesized Bchl a. Strains within the second group (the DFL-35 cluster) formed a new species of Roseovarius and did not produce Bchl a under the conditions investigated here, thus demonstrating the importance of genetic methods for screening of cultivation-dependent metabolic traits. The pufL genes of the dinoflagellate isolates were phylogenetically closely related to pufL genes from Betaproteobacteria, confirming similar previous observations which have been interpreted as indications of gene transfer events.     

Vertical profiles of primary productivity,biomass and physico-chemical properties in meromictic Big Soda Lake,Nevada, U.S.A.

The contribution of bacteria to total primary production was estimated in Big Soda Lake and related to vertical profiles of biomass and various physical and chemical properties. The purple sulfur bacteriaThiocapsa sp. was responsible for 25% of the total primary production. Bacteriochlorophyll (BChl) distribution and DCMU sensitivity experiments confirmed this bacterial activity. High concentrations of photosynthetically inactive phytoplankton were detected in anaerobic-low redox water and were attributed to an early season algal bloom that had settled into a zone of maximal viscosity. Nutrient enrichment bioassay experiments indicated that iron was the most important nutrient controlling early season algal growth.     

Host-Specificity and Dynamics in Bacterial Communities Associated with Bloom-Forming Freshwater Phytoplankton

Many freshwater phytoplankton species have the potential to form transient nuisance blooms that affect water quality and other aquatic biota. Heterotrophic bacteria can influence such blooms via nutrient regeneration but also via antagonism and other biotic interactions. We studied the composition of bacterial communities associated with three bloom-forming freshwater phytoplankton species, the diatom Aulacoseira granulata and the cyanobacteria Microcystis aeruginosa and Cylindrospermopsis raciborskii. Experimental cultures incubated with and without lake bacteria were sampled in three different growth phases and bacterial community composition was assessed by 454-Pyrosequencing of 16S rRNA gene amplicons. Betaproteobacteria were dominant in all cultures inoculated with lake bacteria, but decreased during the experiment. In contrast, Alphaproteobacteria, which made up the second most abundant class of bacteria, increased overall during the course of the experiment. Other bacterial classes responded in contrasting ways to the experimental incubations causing significantly different bacterial communities to develop in response to host phytoplankton species, growth phase and between attached and free-living fractions. Differences in bacterial community composition between cyanobacteria and diatom cultures were greater than between the two cyanobacteria. Despite the significance, major differences between phytoplankton cultures were in the proportion of the OTUs rather than in the absence or presence of specific taxa. Different phytoplankton species favoring different bacterial communities may have important consequences for the fate of organic matter in systems where these bloom forming species occur. The dynamics and development of transient blooms may also be affected as bacterial communities seem to influence phytoplankton species growth in contrasting ways.     

Analysis of bacterial communities in a municipal duck pond during a phytoplankton bloom and isolation of Anatilimnocola aggregata gen. nov., sp. nov., Lacipirellula limnantheis sp. nov. and Urbifossiella limnaea gen. nov., sp. nov. belonging to the phylum Planctomycetes

Waterbodies such as lakes and ponds are fragile environments affected by human influences. Suitable conditions can result in massive growth of phototrophs, commonly referred to as phytoplankton blooms. Such events benefit heterotrophic bacteria able to use compounds secreted by phototrophs or their biomass as major nutrient source. One example of such bacteria are Planctomycetes, which are abundant on the surfaces of marine macroscopic phototrophs; however, less data are available on their ecological roles in limnic environments. In this study, we followed a cultivation-independent deep sequencing approach to study the bacterial community composition during a cyanobacterial bloom event in a municipal duck pond. In addition to cyanobacteria, which caused the bloom event, members of the phylum Planctomycetes were significantly enriched in the cyanobacteria-attached fraction compared to the free-living fraction. Separate datasets based on isolated DNA and RNA point towards considerable differences in the abundance and activity of planctomycetal families, indicating different activity peaks of these families during the cyanobacterial bloom. Motivated by the finding that the sampling location harbours untapped bacterial diversity, we included a complementary cultivation-dependent approach and isolated and characterized three novel limnic strains belonging to the phylum Planctomycetes.     

Viral impacts on total abundance and clonal composition of the harmful bloom-forming phytoplankton Heterosigma akashiwo

Recent observations that viruses are very abundant and biologically active components in marine ecosystems suggest that they probably influence various biogeochemical and ecological processes. In this study, the population dynamics of the harmful bloom-forming phytoplankton Heterosigma akashiwo (Raphidophyceae) and the infectious H. akashiwo viruses (HaV) were monitored in Hiroshima Bay, Japan, from May to July 1998. Concurrently, a number of H. akashiwo and HaV clones were isolated, and their virus susceptibilities and host ranges were determined through laboratory cross-reactivity tests. A sudden decrease in cell density of H. akashiwo was accompanied by a drastic increase in the abundance of HaV, suggesting that viruses contributed greatly to the disintegration of the H. akashiwo bloom as mortality agents. Despite the large quantity of infectious HaV, however, a significant proportion of H. akashiwo cells survived after the bloom disintegration. The viral susceptibility of H. akashiwo isolates demonstrated that the majority of these surviving cells were resistant to most of the HaV clones, whereas resistant cells were a minor component during the bloom period. Moreover, these resistant cells were displaced by susceptible cells, presumably due to viral infection. These results demonstrated that the properties of dominant cells within the H. akashiwo population change during the period when a bloom is terminated by viral infection, suggesting that viruses also play an important role in determining the clonal composition and maintaining the clonal diversity of H. akashiwo populations. Therefore, our data indicate that viral infection influences the total abundance and the clonal composition of one host algal species, suggesting that viruses are an important component in quantitatively and qualitatively controlling phytoplankton populations in natural marine environments.